Mapping the Diversity of Microbial Lignin Catabolism: Experiences from the Elignin Database

Applied Microbiology and Biotechnology (2019) 103:3979–4002 https://doi.org/10.1007/s00253-019-09692-4

MINI-REVIEW

Mapping the diversity of microbial lignin catabolism: experiences from the eLignin database

Daniel P. Brink1 & Krithika Ravi2 & Gunnar Lidén2 & Marie F Gorwa-Grauslund1

Received: 22 December 2018 /Revised: 6 February 2019 /Accepted: 9 February 2019 /Published online: 8 April 2019 # The Author(s) 2019

Abstract Lignin is a heterogeneous aromatic biopolymer and a major constituent of lignocellulosic biomass, such as wood and agricultural residues. Despite the high amount of aromatic carbon present, the severe recalcitrance of the lignin macromolecule makes it difficult to convert into value-added products. In nature, lignin and lignin-derived aromatic compounds are catabolized by a consortia of microbes specialized at breaking down the natural lignin and its constituents. In an attempt to bridge the gap between the fundamental knowledge on microbial lignin catabolism, and the recently emerging field of applied biotechnology for lignin biovalorization, we have developed the eLignin Microbial Database (www.elignindatabase.com), an openly available database that indexes data from the lignin bibliome, such as microorganisms, aromatic substrates, and metabolic pathways. In the present contribution, we introduce the eLignin database, use its dataset to map the reported ecological and biochemical diversity of the lignin microbial niches, and discuss the findings.

Keywords Lignin . Database . Aromatic metabolism . Catabolic pathways . Bioconversion . Ecological niche

Introduction microbial depolymerization (Ruiz-Dueñas and Martínez 2009). Various types of lignin streams (here called technical Lignin is one of the three main components in lignocellulosic lignins) are produced in high amounts in the pulp and paper biomass and the most abundant terrestrial aromatic macromol- industry and are today primarily used to generate process ecule and is as such a potentially great source of renewable steam and electricity by incineration (Li and Takkellapati aromatic compounds (Holladay et al. 2007). It is found in the 2018; Naqvi et al. 2012). These lignin streams are therefore cell walls of lignocellulosic plants (Fig. 1), where it is a largely untapped resource for sustainable production of plat- intertwined with the other two main polymers (cellulose and form chemicals and have the potential to become a key feed- hemicellulose), and confers structural strength, impermeabili- stock in a future expanded biorefinery concepts (Beckham ty, and water transport in the cell wall (Ayyachamy et al. et al. 2016). 2013). The main characteristic traits of the lignin Microbial lignin degradation in nature has been studied for macropolymer are its highly amorphous structure—caused decades, with the scientific literature stretching back to at least by the high heterogeneity of its aromatic building blocks (in the 1960s and studies on, e.g., Pseudomonas putida (Ornston turn directly depending on the plant species) (Gellerstedt and and Stanier 1966). Due to the high diversity of the lignin Henriksson 2008;LewisandYamamoto1990; Vanholme heteropolymer, the microbial modes of lignin catabolism are et al. 2010)—and its severe recalcitrance to chemical and also diverse (Bugg et al. 2011b; Durante-Rodríguez et al. 2018; Fuchs et al. 2011). Lignin degraders are typically bacteria and fungi: among the former, the species mostly belong to the Actinobacteria and Proteobacteria phyla (Bugg et al. * Daniel P. Brink [email protected] 2011b;Tianetal.2014); as for the fungi, the common degraders are of the white rot fungi, filamentous fungi, and yeast taxa (Durham et al. 1984; Guillén et al. 2005; Martins et al. 1 Applied Microbiology, Department of Chemistry, Lund University, P.O. Box 124, SE-221 00 Lund, Sweden 2015). Furthermore, the lignin recalcitrance often prevents one single species from fully degrading the lignin polymer, 2 Department of Chemical Engineering, Lund University, Lund, Sweden and instead a symbiosis where rot-type fungi and bacteria are 3980 Appl Microbiol Biotechnol (2019) 103:3979–4002

Fig. 1 Schematic representation of the lignin microbial niche. In this enzymatic depolymerization (subgroup 2). There is also some overlap model of the niche, lignin is mineralized by two subgroups: lignolytic between the subgroups, with species capable of both lignolysis and species and aromatic degrading species. Some species degrade or modify aromatic degradation. Yellow circles represent the different origins of lignin to access the hemi-/cellulose on which they grow (subgroup 1), and isolation reported for this niche. The poplar lignin structure was adapted other species catabolize the aromatic lignin fragments that result from the from Vanholme et al. (2010) working together is needed to achieve a complete degradation On the applied side, chemical depolymerization of natural (Cragg et al. 2015; de Boer et al. 2005), thus generating a or technical lignins is required to establish a biotechnological specific niche (Fig. 1) that selects for a small set of microbial value chain from mono- or oligoaromatics. The lignin streams, genera. e.g., from the pulp and paper industry, must be depolymerized Appl Microbiol Biotechnol (2019) 103:3979–4002 3981 to yield mono- and oligomeric aromatic compounds microbial lignin catabolism. A literature survey showed that (Ragauskas et al. 2014; Zakzeski et al. 2010) that are then there have been published databases on lignin biochemistry in fed to suitable microbes (natural or engineered) for bioconver- the past, but they are, at the time of writing, all unavailable sion into value-added products. However, most knowledge on and/or discontinued: FOLy, a database on fungal oxidoreduc- the microbial side of this process comes from natural de- tases for lignin catabolism (Levasseur et al. 2008); LD2L, a graders, and little is currently known about microbial growth database similar in scope as eLignin (Arumugam et al. 2014); and utilization on the cocktail of aromatic compounds found and an NMR database for lignin structures (Ralph et al. 2004), in depolymerized technical lignin. Furthermore, although dif- with the latter not treating microbial catabolism. The objective ferent lignocellulosic feedstocks (e.g., softwood, hardwood, of eLignin is to collect data on strains of microorganisms agricultural residues) are known to contain different amounts (bacteria, yeasts, and fungi) known to degrade and/or catabo- and types of aromatic building blocks (Gellerstedt and lize lignin and lignin-derived aromatic compounds. Henriksson 2008; Ragauskas et al. 2014), it is very challeng- Specifically, the database content includes microorganisms, ing to predict the chemical composition of the mixture substrates, pathways, genes, metabolic reactions, and en- resulting from a depolymerization process, especially for tech- zymes related to the topic (Table 1). So far, its prime focus nical lignins (Abdelaziz et al. 2016). Consequently, it is diffi- has been on collecting data on microbial diversity and cult to a priori select a suitable microbial host until chemical intracellular events; however, the database can later be ex- analysis has been performed on the depolymerized (low mo- panded with extracellular enzymes and reactions (such as lecular weight) lignin stream. laccases and peroxidases), as these play an important role in The literature on microbial lignin catabolism is vast and microbial degradation of native lignin and can be applied for combines fundamental microbiology and applied studies that enzymatic depolymerzation of technical lignins (Bourbonnais have in particular seen a surge in popularity during the last et al. 1995; Pardo et al. 2018;Zhaoetal.2016). decade. However, there has been little effort yet to facilitate an In practice, the data in eLignin is retrieved from scientific overview of the large amount of publications in this field, literature (peer-reviewed articles, reviews, and books), manu- especially regarding intracellular microbial events. For this ally curated and supplemented with links to relevant entries in reason, we have created a new database named The eLignin other well-established biological and chemical databases (e.g., Microbial Database (www.elignindatabase.com)for GenBank (Benson et al. 2012), KEGG (Kanehisa and Goto collection of data from scientific literature on the catabolism 2000), PubChem (Kim et al. 2015), and ChEBI (Hastings of lignin and lignin-derived aromatic compound by microor- et al. 2012)). The initial dataset was collected by performing ganisms. The eLignin database was launched online in a systematic literature review according to the Kitchenham March 2017 and aims to bring together the bibliome of this protocol (Kitchenham 2004), where 561 articles (title, ab- field in one self-contained searchable platform, and thus fill a stract, and keywords) were screened and analyzed for their gap presently not covered by other online biological data- inclusion in the database bibliome. Since the eLignin dataset bases, as well as to demonstrate the high diversity of this originates from scientific literature, users are encouraged to microbial niche (Fig. 1). As the database primarily focuses read the primary references for any data of interest, since there on intracellular conversion steps, information on extracellular will be aspects of the data that are not indexed or reviewed by enzymes with lignolytic activities are currently not covered eLignin (such as experimental conditions). Due to the nature and the readers are redirected to, e.g., the following reviews of the data collection for eLignin (scientific publications), (Janusz et al. 2017; Sigoillot et al. 2012). there will be some overlap with other biological databases The present minireview will introduce the design philoso- such as MetaCyc (Caspi et al. 2015), GenBank (Benson phy of the eLignin database and present our outcome of the et al. 2012), or UniProt (UniProtConsortium 2017), when it diversity analysis with prime focus on intracellular microbial comes to information on pathways, genes, and enzymes. As events. What sets this paper apart from other recent reviews we do not strive to master features that already established discussing the diversity of microbial lignin degradation (Bugg databases already do, eLignin entries are annotated with links et al. 2011a;Tianetal.2014) is that we have been able to use to specialized databases where possible. the established content of the database (Table 1)tomakepat- Two major entry points were considered for eLignin: a tern recognitions over the indexed publications in eLignin (for microorganism- and a substrate-oriented search (Fig. 2). instance using relational SQL queries and Python scripts). This design choice was made in order to cater to what we foresee are the two most common information needs both in fundamental and applied lignin microbial conversion: (i) Scope and design of the eLignin database What substrates can my microbe of choice breakdown and/ or utilize?; (ii) What microorganism can I use to consume the The eLignin database was created because there is, to our lignin and lignin-derived aromatics in my substrate stream? knowledge, no currently available database dedicated to Using these entry points, we will now describe the current 3982 Appl Microbiol Biotechnol (2019) 103:3979–4002

Table 1 Content of the eLignin database as of the time of writing Entry Count

Organisms 261 organisms (171 prokaryotes, 85 eukaryotes, 5 archaea) Substrates 141 Metabolic pathways 26 Genes 90 Enzymes 59 Reactions 76 Total entries 653 References 330

Please note that these figures are subject to increase over time, as more data and references (both past and newly published scientific literature) are continuously added state of the bibliome and use eLignin content to map and lignocellulose degraders is so far limited to a few bacterial and discuss the presently known diversity of the lignin microbial fungal phyla (Janusz et al. 2017; Tian et al. 2014). niche. Mineralization of the lignin requires two main steps: (1) breakdown of the lignin macropolymer to yield smaller aromatic compounds and (2) ring fission of the resulting aromatic The microbial diversity in the lignin niche, compounds (Tuor et al. 1995). The first step is carried out by as reported in the eLignin bibliome microbes able to secrete extracellular enzymes with lignolytic and/or lignin-modifying activities such as laccases and Lignocellulose degradation through cellulolytic activity has peroxidases—typically wood-decaying fungi and certain bac- been found to be distributed in a wide range of genera within terial species (Bugg et al. 2011b;Januszetal.2017;Sigoillot the Bacteria, Archaea, Fungi, and Animalia kingdoms (Cragg et al. 2012)(Fig.1). The resulting heterogeneous mixture of et al. 2015). However, the known lignin-degrading subset of aromatic breakdown products is then metabolized by the

Fig. 2 Schematic overview of the eLignin database. The figure illustrates that eLignin is a microorganism- and substrate-focused database and that every entry type (organism, substrate, gene, enzyme, pathway, reaction) is accessible from each of these point-of-entries Appl Microbiol Biotechnol (2019) 103:3979–4002 3983 lignolytic secreters themselves or by other microorganisms in (Tables 2 and 3). Evidence of some aromatic-degrading ar- the vicinity capable of aromatic catabolism (Cragg et al. chaea (of the kingdom of Euryarchaeota) is also beginning 2015). This leads to the establishment of a microbial niche to emerge (Emerson et al. 1994;Erdoğmuş et al. 2013; that favors microbes with matching substrate specificity for Khemili-Talbi et al. 2015). Overall, the large occurrence of the resulting aromatic compounds and with tolerance to the Proteobacteria is noteworthy, and the species of this phylum often inhibitory or toxic nature of the aromatics (Díaz et al. are indeed enriched in studies of isolates found from lignin- 2013; Krell et al. 2012; Schweigert et al. 2001). During catab- rich environments and selected on growth on lignin and aro- olism, the aromatic breakdown products are typically shunted matic compounds (Jimenez et al. 2002; Jurková and Wurst through a number of reactions that are collectively referred to 1993; Kuhnigk and Konig 1997; Narbad and Gasson 1998; as funneling pathways (Harwood and Parales 1996)—or Overhage et al. 1999; Perestelo et al. 1996;Ravietal.2017). sometimes upper pathways (Linger et al. 2014)—that eventu- Likewise, when the same organisms were analyzed for their ally converge on a couple of conserved ring fission pathways origin of isolation, it was clear that a majority originated from where the aromatic rings are cleaved and the subsequent me- soil and from the forest ground layer (Table 4), which is prob- tabolites enter the central carbon metabolism (Fuchs et al. ably the most expected ecosystem for the lignin microbial 2011). Because of these two main steps (depolymerization niche (Cragg et al. 2015; Harwood and Parales 1996)given and ring fission), the lignin microbial niche can be said to the abundance of lignocellulose in different states of decay contain two main groups of microbes: lignin macropolymer found in there. degraders and degraders of lignin-derived aromatic com- The following subsections will discuss the outcome of the pounds (with the former often being capable of the latter analysis of the database content in terms of fungal, bacterial, (Nakamura et al. 2012)), from here on referred to as niche and archaeal diversity. Also, in order to complement the pure subgroups 1 and 2 (Fig. 1). The eLignin database aims to isolate approach of the database, the last subsection will dis- index both, and for the remainder of the minireview, the con- cuss microbial communities. cept of the lignin microbial niche will be used to refer to all microbes that are capable of degrading lignin and lignin- Fungal diversity derived aromatic compounds. Subgroup 2 is of importance for applied studies aiming to, e.g., valorize chemically The fungi listed in the database are either of the wood rot-type depolymerized lignin, or to perform in situ bioremediation, or yeasts. Wood-decaying, or wood-rot, fungi are found within and thus, an extra effort has been put on this group in the the Basidiomycota and Ascomycota phyla and can be divided eLignin database. into three different types that all have lignin-modifying activ- Within the applied side of lignin bioconversion, a quick ities to various extent: soft-rot, brown-rot, and white-rot fungi survey of the recent literature shows that a substantial amount (Hatakka 2005; Janusz et al. 2017). Soft-rot fungi tend to of research articles focus on a few commonly used model prefer hardwood and seem to only weakly affect lignin organisms such as Pseudomonas putida (Linger et al. 2014), (Sigoillot et al. 2012), but a few species have been reported Sphingobium sp. (Masai et al. 1999), Rhodococcus jostii to exhibit white-rot–like activity toward the end of the wood (Sainsbury et al. 2013), and Rhodococcus opacus (Kosa and decay (Pildain et al. 2005). Brown-rot fungi, which are mainly Ragauskas 2012). Reviews on microbial lignin degradation found in the Basidiomycota phylum, selectively attack hemi- that often include large tables with important isolates cellulose and cellulose and leave a modified (e.g., dealkylated, (Abdelaziz et al. 2016;Buggetal.2011a;Tianetal.2014) demethoxylated, and/or demethylated) lignin signified by its are seldom listing more than ~ 50 different microbes. Still, brown color (hence the name of this group of wood de- over 250 microorganisms with lignin and lignin-derived aro- graders); they are primarily found in softwood ecosystems matics catabolic activity are currently mapped in the eLignin (Hatakka 2005; Sigoillot et al. 2012). Finally, white-rot fungi bibliome (Tables 1, 2,and3), which indicates its usefulness can degrade all three main components of lignocellulose, i.e., for meta-analysis of the field. hemicellulose, cellulose, and lignin, and leave a decayed The listed species in the current dataset of eLignin are wood with a bleached color (Blanchette 1984; Eriksson et al. distributed over 90 different genera, which in turn can be 1980; Sigoillot et al. 2012). White-rots are the only wood- classified into six bacterial phyla (Acidobacteria, decaying fungi that can completely degrade lignin to CO2 Actinobacteria, Bacteroidetes, Firmicutes, Proteobacteria, and H2O; however, it has been proposed that lignin cannot and Spirochaetes) and two fungal phyla (Ascomycota and be used as the sole carbon source by white-rots; rather, the Basidiomycota) (see Tables 2 and 3). However, the majority lignin degradation is probably a process that the fungi use to of the microbes belong to five of the eight observed phyla: access the cellulose and hemicellulose (ten Have and Proteobacteria (114 species/strains), Basidiomycota (58 spe- Teunissen 2001). Like brown-rot fungi, white-rot fungi mostly cies/strains), Actinobacteria (31 species/strains), Ascomycota belong to the Basidiomycota phylum and to a smaller extent to (27 species/strains), and Firmicutes (22 species/strains) the Ascomycota (Sigoillot et al. 2012). 3984 Appl Microbiol Biotechnol (2019) 103:3979–4002

Table 2 Distribution of bacterial genera in the dataset of known degraders of lignin and/or lignin-derived aromatics index in the eLignin database

Genus (sorted by Number of species References phylum) in eLignin

Acidobacteria (Gram stain differs with species) Holophaga 1Baketal.(1992) Actinobacteria (Gram-positive) Amycolatopsis 1 Sutherland (1986) Arthrobacter 1 Kerr et al. (1983) Corynebacterium 1 Qi et al. (2007) Microbacterium 1Song(2009), Taylor et al. (2012) Micrococcus 1Tayloretal.(2012) Nocardia 2 Crawford et al. (1973), Kuhnigk and Konig (1997) Pelobacter 1 Schink and Pfennig (1982) Rhodococcus 11 Chong et al. (2018), Chung et al. (1994), Eulberg et al. (1997), Henson et al. (2018), Karlson et al. (1993), Kosa and Ragauskas (2012), Sainsbury et al. (2013), Song (2009), Taylor et al. (2012) Streptomyces 10 Antai and Crawford (1981), Aoyama et al. (2014), Chow et al. (1999), Davis and Sello (2010), Giroux et al. (1988), Ishiyama et al. (2004), Kuhnigk and Konig (1997), Watanabe et al. (2003), Yang et al. (2012), Zeng et al. (2013) Thermobifida 1Changetal.(2014) Thermomonospora 1 McCarthy and Broda (1984) Bacteroidetes (Gram-negative) Dysgonomonas 1 Duan et al. (2016b) Sphingobacterium 1Tayloretal.(2012) Firmicutes (mostly Gram-positive) Acetoanaerobium 1 Duan et al. (2016a) Acetobacterium 2 Bache and Pfennig (1981), Kaufmann et al. (1998) Aneurinibacillus 1 Raj et al. (2007) Bacillus 10 Chandra et al. (2007), Huang et al. (2013), Kuhnigk and Konig (1997), Perestelo et al. (1989), Zhu et al. (2017) Brevibacillus 2Hoodaetal.(2015, 2018) Clostridium 2 Daniel et al. (1988), Mechichi et al. (1999) Paenibacillus 3Chandraetal.(2007), Crawford et al. (1979), Mathews et al. (2014) Papillibacter 1 Defnoun et al. (2000) Spirochaetes (Gram stain differs with species) Treponema 1 Lucey and Leadbetter (2014) Proteobacteria (Gram-negative) Achromobacter 1Benjaminetal.(2016) Acinetobacter 7 Delneri et al. (1995), Fischer et al. (2008), González et al. (1993), Kuhnigk and Konig (1997), Mazzoli et al. (2007), Van Dexter and Boopathy (2018), Vasudevan and Mahadevan (1992) Aeromonas 2 Deschamps et al. (1980), Gupta et al. (2001) Agrobacterium 1 Parke (1997) Alcaligenes 1 Kuhnigk and Konig (1997) Aromatoleum 1 Rabus and Widdel (1995) Azoarcus 1 Gorny et al. (1992) Azotobacter 2 Hirose et al. (2013), Groseclose and Ribbons (1981) Bradyrhizobium 1 Sudtachat et al. (2009) Burkholderia 7 Hamzah and Al-Baharna (1994), Harazono et al. (2003), Kato et al. (1998), Kuhnigk and Konig (1997), Song (2009), Woo et al. (2014b), Yang et al. (2017) Citrobacter 3 Chandra and Bharagava (2013), Harazono et al. (2003) Appl Microbiol Biotechnol (2019) 103:3979–4002 3985

Table 2 (continued)

Genus (sorted by Number of species References phylum) in eLignin

Comamonas 5 Chen et al. (2012c), Kamimura et al. (2010), Kuhnigk and Konig (1997), Ni et al. (2013), Providenti et al. (2006) Cupriavidus 5 Hughes and Bayly (1983), Perez-Pantoja et al. (2008), Sato et al. (2006),Shietal.(2013a) Desulfobacterium 2BakandWiddel(1986), Szewzyk and Pfennig (1987) Enterobacter 5 DeAngelis et al. (2013), Deschamps et al. (1980), Grbić-Galić (1985), Yoshida et al. (2010) Flavimonas 1Song(2009) Flavobacterium 1 Hirose et al. (2013) Klebsiella 4 Hirose et al. (2013), Jones and Cooper (1990), Woo et al. (2014a), Xu et al. (2018) Marinobacterium 1Gonzálezetal.(1997) Mesorhizobium 1 Tian et al. (2016) Microbulbifer 1Gonzálezetal.(1997) Moraxella 1 Novosphingobium 2 Chen et al. (2012b), Liu et al. (2005) Oceanimonas 1 Numata and Morisaki (2015) Ochrobactrum 6 Hirose et al. 2013), Kuhnigk and Konig (1997), Taylor et al. (2012), Tsegaye et al. (2018), Xu et al. (2018) Pandoraea 3 Bandounas et al. (2011), Kumar et al. (2015), Shi et al. (2013b) Pantoea 3Song(2009), Xiong et al. (2014), Zeida et al. (1998) Pseudomonas 27 Chapman and Ribbons (1976), Chowdhury et al. (2004), Cronin et al. (1999), Gao et al. (2005), Hirose et al. (2013), Hirose et al. (2018), Iwabuchi et al. (2015), Jimenez et al. (2002), Jurková and Wurst (1993), Kuhnigk and Konig (1997), Li et al. (2010), Mahiudddin and Fakhruddin (2012), Maruyama et al. (2004), Murray et al. (1972), Narbad and Gasson (1998), Nikodem et al. (2003), Ornston and Parke (1976), Overhage et al. (1999), Perestelo et al. (1996), Ravi et al. (2018), Shettigar et al. (2018), Tian et al. (2016), Xu et al. (2018) Rhizobium 1 Jackson et al. (2017) Rhodopseudomonas 2 Harwood and Gibson (1988), Salmon et al. (2013) Sagittula 1Gonzalezetal.(1997) Serratia 5 Haq et al. (2016), Perestelo et al. (1990), Rhoads et al. (1995), Tian et al. (2016) Sinorhizobium 1 MacLean et al. (2006) Sphingobium 1Masaietal.(2007) Sphingomonas 1Balkwilletal.(1997) Stenotrophomonas 1 Tian et al. (2016) Sulfuritalea 1 Sperfeld et al. (2018) Thauera 2 Mechichi et al. (2005), Tschech and Fuchs (1987) Tolumonas 1 Billings et al. (2015) Trabulsiella 1 Suman et al. (2016)

Both brown-rot and white-rot fungi invade the wood cell the highly variable tertiary structure of lignin could explain lumen by hyphal growth and secrete their lignocellolytic en- why no nucleophilic lignolytic enzymes have been described zymes (Kirk and Farrell 1987; Leonowicz et al. 1999). The (Hammel and Cullen 2008). The level and patterns of decay lignolytic mechanisms of white-rot fungi secretome have been vary between different fungal species and the type of wood thoroughly studied (Leonowicz et al. 1999; ten Have and (Worrall et al. 1997) as well as the state of decay of the wood. Teunissen 2001). The known lignolytic enzymes (e.g., lignin Fukasawa and colleagues subjected beech wood in varying peroxidases, manganese peroxidases, versatile peroxidases, levels of decay to different fungal species and were able to and laccases (Janusz et al. 2017)) work by nonspecific oxida- demonstrate that the Basidiomycota caused its highest weight tion, and although nucleophilic cleavage can be used for loss in nondecayed wood, whereas the assayed Ascomycota chemical depolymerization of lignin (e.g., in kraft pulping), caused more weight loss in predecayed wood (Fukasawa et al. 3986 Appl Microbiol Biotechnol (2019) 103:3979–4002

Table 3 Distribution of fungal genera in the dataset of known degraders of lignin and/or lignin-derived aromatics index in the eLignin database

Genus (sorted by phylum) Number of species in eLignin References

Ascomycota Aspergillus 3 Barapatre and Jha (2017), Martins et al. (2015), Yang et al. (2011) Brettanomyces 1 Edlin et al. (1995) Candida 7 Fialova et al. (2004), Gérecová et al. (2015), Krug et al. (1985) Emericella 1 Barapatre and Jha (2017) Exophiala 1 Middelhoven (1993) Fusarium 5 Chang et al. (2012), Falcon et al. (1995), Korniłłowicz-Kowalska and Rybczyńska (2015), Michielse et al. (2012) Oudemansiella 1Fukasawaetal(2011) Geotrichum 1 Sláviková and Košíková (2001) Penicillium 1 Rodriguez et al. (1994) Pestalotia 1Falconetal.(1995) Petriellidium 1 Eriksson et al. (1984) Phialophora 1 Eriksson et al. (1984) Phoma 1Bietal.(2016) Trichoderma 3 Korniłłowicz-Kowalska and Rybczyńska (2015), Ryazanova et al. (2015) Basidiomycota Agaricus 1 Saha et al. (2016) Anthracophyllum 1 Acevedo et al. (2011) Auricularia 1 Liers et al. (2011) Bjerkandera 3 Fukasawa et al. (2011), Liers et al. (2011), Saha et al. (2016) Ceriporiopsis 1 Rüttimann-Johnson et al. (1993) Cryptococcus 1 Bergauer et al. (2005) Cyathus 3 Saha et al. (2016), Sethuraman et al. (1999) Daedalea 1 Arora and Sandhu (1985) Hymenochaete 1 Saito et al. (2018) Dichomitus 1PériéandGold(1991) Irpex 2 Saha et al. (2016), Xu et al. (2009) Leucosporidium 1 Middelhoven (1993) Marasmius 1 Saito et al. (2018) Mastigobasidium 1 Bergauer et al. (2005) Microbotryomycetidae 1 Bergauer et al. (2005) Mycena 1 Liers et al. (2011) Nematoloma 1 Hofrichter et al. (1999) Phanerochaete 4 Eriksson et al. (1983), Hiratsuka et al. (2005), Saha et al. (2016), Vares et al. (1994) Phlebia 5Bietal.(2016), Liers et al. (2011), Saito et al. (2018), Vares et al. (1994) Pleurotus 1 Liers et al. (2011) Polyporus 1 Saha et al. (2016) Pycnoporus 3 Eggert et al. (1996), Saha et al. (2016) Rhodosporidium 2 Bergauer et al. (2005), Yaegashi et al. (2017) Rhodotorula 8 Bergauer et al. (2005), Durham et al. (1984), Gupta et al. (1986), Hainal et al. (2012), Huang et al. (1993), Sampaio (1999) Rigidoporus 1 Saha et al. (2016) Sporobolomyces 1 Bergauer et al. (2005) Stropharia 2 Liers et al. (2011), Saito et al. (2018) Trametes 3 Alexieva et al. (2010), Fukasawa et al. (2011), Knežević et al. (2018) Trichosporon 4 Middelhoven 1993), Sietmann et al. (2001), Sláviková et al. (2002), Yaguchi et al. (2017) Appl Microbiol Biotechnol (2019) 103:3979–4002 3987

Table 4 Origin of isolation of the 261 organisms listed in the eLignin When it comes to lignin-degrading activity, fungi tend to be database as of November 2018 more studied than bacteria because of their higher prevalence Origin of isolation Number of organisms of lignolytic secretomes (Janusz et al. 2017). However, if the system boundaries are expanded to include the whole lignin Total Bacteria Fungi Archaea aromatic niche, i.e., the species that lack delignification activities but grow on the lignin-derived aromatic compounds (Fig. Aquatic 8 5 1 2 1), the ratio between fungi and bacteria could be rather differ- Caves and mines 6 1 5 0 ent. In eLignin, which was built on this niche principle, there Clinical isolate 6 0 6 0 are about two times as many bacterial isolates listed as fungal Compost 5 5 0 0 ones (Tables 1, 2,and3). We cannot determine if this is a bias Forest and wood samples 40 17 23 0 in the literature, comes from the database boundaries (which Industrial plants 5 1 2 2 were initially created with a focus on intracellular events, and Lab-made derivative 4 4 0 0 not on secreted enzymes), or if the Btrue^ diversity holds less Other 2 1 1 0 fungal species than bacterial. The number of wood-rotting Pulp and paper mill effluent 16 15 1 0 Basidiomycetes has been estimated to up to 1700 species in Sediment 15 15 0 0 North America only, but the number of lignolytic fungi is Seeds and hulls 2 2 0 0 unknown (Gilbertson 1980;Januszetal.2017). Soil 92 70 21 1 Termite gut 22 22 0 0 Bacterial diversity Unknown or not specified 27 3 24 0 Wastewater sludge 11 10 1 0 By using the holistic ecological approach to list both de- The organisms have been sorted in 15 main clusters in order to facilitate graders of lignin and lignin-derived aromatic compounds, the clustering, and the specific details can be found in the database entry 171 different bacteria distributed over 63 different genera have for each organism been indexed in eLignin at the time of writing (Table 2). As mentioned above, three main phyla encompasses the bulk of 2011), which implicates that there is a sequential order within the dataset (Proteobacteria, Actinobacteria,andFirmicutes), the lignin microbial niche with different types of fungi taking with Proteobacteria dominating the list with its 114 entries turns for degrading the (residual) wood. A very thorough (Table 2). Within these Proteobacteria, γ-Proteobacteria was indexing of microbes (primarily fungi) that secrete lignolytic the main class (66 species/strains), followed by β- enzymes can be found in a supplemental table of the review of Proteobacteria (27 species/strains), α-Proteobacteria (18 Janusz et al. (2017). species/strains), and δ-Proteobacteria (3 species/strains), The 85 eukaryotes (fungi and yeasts from 43 different gen- again highlighting that certain types of microbes are greatly era) currently listed in eLignin are distributed between enriched in the eLignin bibliome. It can also be noted that Ascomycota and Basidiomycota (Table 3) and were primarily many of the organisms in this particular niche have undergone isolated from soil and forest environments (Table 4), which is one or several taxonomical reclassifications since they were in accordance with other reviews of the ecological occurrence first isolated and described (see, e.g., Cupriavidus necator (Janusz et al. 2017). The clinical isolates reported in Table 4 which was previously known as, e.g., Ralstonia eutropha are mainly different species of Candida yeasts, which aside and Wautersia eutropha (Vandamme and Coenye 2004)), from their opportunistic pathogenicity in humans, are known meaning that the binomial names in articles from the 1960– degraders of lignocellulose-derived compounds such as xy- 1980s may be different from the currently prevailing names. lose and different aromatics (Gérecová et al. 2015;Holesova Therefore, the organism entry in the database has, when pos- et al. 2011; Jeffries 1981;Krugetal.1985). In general, the sible, been harmonized with links to the corresponding entry yeasts species in the database are aromatic degraders and not in the NCBI Taxonomy Database (https://www.ncbi.nlm.nih. lignin degraders (Bergauer et al. 2005;Holesovaetal.2011; gov/taxonomy; Acland et al. 2014). Middelhoven 1993; Yaegashi et al. 2017) and, therefore, play The Gram stain distribution tends to follow the phyla and, a role in the niche as degraders of lignin breakdown products. thus, is dominated by Gram-negative bacteria (121 species/ Three species in the dataset have, however, been reported to strains), with the remainder being Gram-positive (46 species/ have activity on lignin: Rhodotorula sp. R2 modified wheat strains) and unknown/Gram-indeterminate (4 species/strains). straw and Sarkanda grass (Hainal et al. 2012), whereas This may have implication on studies focusing on, e.g., trans- Geotrichum klebahnii CCY 74-6-2 and Trichosporon port of compounds over membranes (discussed in a separate pullulans CCY 30-1-10 acted on beechwood lignin fraction- section below), or when expanding a species’ substrate range ated from the prehydrolysis step of kraft pulping (Sláviková by metabolic engineering. In the latter case, the difference in and Košíková 2001; Sláviková et al. 2002). total GC content in the genome that is in general seen between 3988 Appl Microbiol Biotechnol (2019) 103:3979–4002

Gram-positives and Gram-negatives (Muto and Osawa 1987) (Durante-Rodríguez et al. 2018). Some examples found in will affect the feasibility of heterologous expression if using the database include, e.g., Pelobacter acidigallici Ma Gal2 traditional PCR-based cloning. (Schink and Pfennig 1982), Desulfobacterium phenolicum Although fungi are known as the main degraders of the Ph01 (Bak and Widdel 1986), Rhodopseudomonas palustris lignin macropolymer (as described in the previous subsec- CGA001 (Harwood and Gibson 1988), Clostridium tion), there are a substantial number of studies that describe thermoaceticum ATCC 39073 (Daniel et al. 1988), and delignifying bacteria. Tian et al. reviewed the topic and per- Dysgonomonas sp. WJDL-Y1 (Duan et al. 2016b); formed phylogeny on 57 lignin-degrading and 463 laccase- Holophaga foetida TMBS4 is also worthy of mention as it encoding prokaryotes that led them to propose that screening the only observed species in the Acidobacteria phylum report- for laccases genes may be a good way to detect new lignin- ed in the database, and it grows anaerobically on a couple of degrading species (Tian et al. 2014). Furthermore, the authors typically lignin-derived aromatics such as ferulic acid and suggest that aromatic metabolism is a prerequisite for but not a syringic acid (Bak et al. 1992). proof of lignolytic activity (Tian et al. 2014), which is in line with our division of the lignin bacterial niche into subgroups 1 Archaeal diversity and 2 that specialize in different aspects of the full lignin catabolism (Fig. 1). The metabolism of the resulting lignin Of the three domains in the Woeseian system (Woese et al. breakdown products, which mainly takes place intracellularly, 1990), archaea is the most underrepresented in the lignin mi- will be discussed in the BDistribution of metabolic pathways crobial niche. To our knowledge, there are no reported archae- and substrate specificities^ section below. al single culture isolates with lignolytic capacity at the time of Soil is absolutely the most common origin of isolation writing. Recently, by enrichment cultures from estuarine sed- mapped in the database (Table 4), which also reflects how iment, it was possible to infer growth of Bathyarchaeota on popular this environment has been for studies on isolation of alkali lignin by the increase in gene-copy number and the lignin and aromatic degraders. Other than soil, termite guts are incorporation of inorganic carbon in the archaeal lipids over a main origin of isolation. There seems to be no clear evidence 11 months (Yu et al. 2018). Likewise, putative laccase genes that the termites themselves are able to degrade lignin (instead have been reported in some archaeal species (Ausec et al. they live of the hydrolysis products of hemicellulose and cel- 2011;SharmaandKuhad2009;Tianetal.2014). A laccase lulose) (Brune and Ohkuma 2010). The lignin barrier is over- from Haloferax volcanii DS70 has been purified with activity come by the termites by a symbiotic relationship with a di- on model compounds such as syringaldazine and ABTS verse microbial community, e.g., by exosymbiotic fungi and (Uthandi et al. 2010). However, to our understanding, the endosymbiotic gut flora (Maurice and Erdei 2018). Examples in vivo lignolytic activity of these putative and purified of aromatic degrading bacteria isolated from the gut flora in- laccases remains to be assayed. clude Proteobacteria (Harazono et al. 2003; Kuhnigk and Five archaeal isolates—classified in niche subgroup 2 Konig 1997; Suman et al. 2016; Tsegaye et al. 2018;Van (growth on aromatics; Fig. 1)—have so far been indexed in Dexter and Boopathy 2018), Actinobacteria (Chung et al. eLignin, all of them being halophiles, i.e., extremophiles that 1994; Kuhnigk and Konig 1997; Watanabe et al. 2003), and prefer high salt concentration. Haloferax sp. D1227 was iso- Firmicutes (Kuhnigk and Konig 1997), as well as the only lated from soil and grew on benzoic, cinnamic, and Spirochaetes entry in the database (Lucey and Leadbetter phenylpropanoic acid (Emerson et al. 1994). Haloferax sp. 2014). Another enrichment reported in Table 4 for bacteria C-24, Halorubrum ezzemoulense C-46, and Haloarcula sp. is the isolates from different man-made environments. One D1 were isolated from high-saline samples and grew on, example is pulp and paper mill effluents that contain residual e.g., 4-hydroxybenzoic acid (Erdoğmuş et al. 2013; Fairley lignins and aromatics and have been a source of many isolates et al. 2002). Natrialba sp. C21 degraded phenol (Khemili- (Chandra et al. 2007;Duanetal.2016b;Gonzálezetal.1997; Talbi et al. 2015). The halophilic nature of these isolates and Hooda et al. 2015; Mathews et al. 2014; Nishikawa et al. the lack of known lignolytic activity seem to suggest that they 1998;Ravietal.2018); likewise, sludge from waste water contribute with the degradation of aromatic breakdown prod- treatment plants has been a source of a number of isolates, ucts that have ended up in saltwater environments, which some of which are strictly anaerobic (Gorny et al. 1992; could be speculated to be a downstream (or downriver)exten- Mechichi et al. 1999, 2005;Nietal.2013; Traunecker et al. sion of the lignin microbial niche. 1991; Tschech and Fuchs 1987). Anaerobic aromatic degrading bacteria are in a minority The communities of the lignin microbial niche compared to the aerobic fission bacteria and were even for a long time believed to be impossible (Kirk and Farrell 1987). Lignin degradation is a community effort and is in itself often However, with recent advances in the field, the molecular a subpart of a lignocellulose-degrading niche (de Boer et al. biology of these pathways has begun to be understood 2005). Microbial communities—organisms that live and Appl Microbiol Biotechnol (2019) 103:3979–4002 3989 interact within a contiguous environment (Konopka 2009)— to the evolution of a panel of intracellular funneling pathways, are in a way what we are illustrating by looking at the isolates i.e., metabolic routes that connect substituted aromatic com- from the point of the niche subgroups (Fig. 1). It has been pounds with a ring fission pathway leading to the central car- proposed that lignin degradation is more rapid with consortia bon metabolism, often (but not always) via acetyl-CoA than single isolates due to synergism (Wang et al. 2013). (Fig. 3). In this section, the eLignin database was used to Furthermore, studies on fungal–bacterial interactions in the assess the diversity of substrates and metabolic routes within lignin microbial niche have reported examples of commensal- the lignin microbial niche. ism as well as amensalism between certain species: some bacteria have been reported to promote growth of a white-rot Reported substrate specificities fungi when co-cultivated (Harry-asobara and Kamei 2018), and there is a report showing two different white-rot species Similar to how fundamental and applied studies on lignin outcompeting opportunistic bacteria (Folman et al. 2008). At focus on a few model organisms, many studies use a few the moment, consortia are not mapped in eLignin but are nev- common model aromatic model compounds that represent ertheless important for the understanding of the lignin different funneling pathways (e.g., 4-hydroxybenzoic acid, microbiology. vanillic acid, ferulic acid, p-coumaric acid, and benzoic acid) Many studies have reported physiological characterization to evaluate the physiology of the microbial niche (see, e.g., of a community with unknown or partly known composition, Fischer et al. 2008;Gonzálezetal.1997; Kosa and Ragauskas either because it was not possible to isolate single cultures 2012;Ravietal.2017; Vardon et al. 2015). However, from with the desired phenotype—for instance, 99% of the bacteria browsing eLignin, there appears to be a much higher substrate in soil have been estimated to be unculturable (Pham and Kim diversity in this niche than just these model compounds. This 2012)—or because the aim was to study the community effort. is illustrated in Fig. 4a, showing a meta-analysis of the Bmost Examples include communities capable of degrading lignin popular^ substrates in the eLignin bibliome in terms of the (DeAngelis et al. 2011;Wangetal.2013;WuandHe2013), number of different microbes that have been reported in the syringic acid (Kaiser and Hanselmann 1982;Phelpsand literature to degrade them. Evidently, the model aromatics are Young 1997), resorcinol and catechol (Milligan and in the top, which both suggest that they indeed are good model Häggblom 1998), coniferyl alcohol (Grbić-Galić 1983), and compounds for the different funneling pathways and that they plant lignin–soil community studies (Bennett et al. 2015; have been popular choices for the experimental work that has Bradley et al. 2007), to name a few. Many of these studies been published on this topic. In addition, some natural and were reported under anaerobic conditions. technical lignins (corn stover, kraft, Klason, and alkaline lig- Another approach to analyze microbial communities is to nin), Bsynthetic^ oligoaromatics (dehydropolymerisate), and consider the makeup of the metagenome as a unique property dimers (biphenol, benzylvanillin) are among these top 32 sub- of a given community (Konopka 2009). 16S rRNA sequenc- strates (Fig. 4a). The number of microbes in the database that ing can be used to taxonomically identify members of a com- have been reported to degrade natural and technical lignins munity (González et al. 1996). A common methodology is to and di-/oligoaromatics is presented in Fig. 4b. The results divide the results of the 16S rRNA sequencing of a show that fungi are the most prevalent degraders of natural metagenome into operational taxonomic units (OTUs) to at- lignins, which is reasonable given the high diversity of tempt to resolve, e.g., phylum level abundances (Moraes et al. lignolytic fungi. The reported technical lignins include chem- 2018); this is similar to what is done here with the eLignin ically modified lignin polymers as well as chemically database using single isolates (Tables 2 and 3). In addition to depolymerized lignin (i.e., a mixture of both high taxonomical metagenomics, Moraes and colleagues recon- (polymeric) and low molecular weight lignins (mono- and structed draft bacterial genomes from a lignin-degrading con- oligomers)) which explains the high number of bacteria that sortium and could identify conserved domains related to lig- have been reported to grow on technical lignins. Di- and nin degradation in their metagenome (Moraes et al. 2018). oligoaromatic compounds were primarily reported in Proteobacteria in eLignin, but this is likely a literature bias since (model) monoaromatic compounds tend to be more Distribution of metabolic pathways commonly studied across all phyla. Note that there are no and substrate specificities Acidobacteria or Spirocheates in the eLignin bibliome that have been reported to degrade natural/technical lignins and The lignin macropolymer is primarily depolymerized by ex- di-/oligoaromatics. tracellular enzymes secreted by lignolytic microbes. Due to its It is equally important to know the substrates that cannot be heterogeneity, the resulting depolymerization products are used by a given organism, as this will give the limitations of its commonly a mixture of different mono- and di- and metabolism. In fact, many isolation papers both list substrates oligoaromatic compounds (Bugg et al. 2011b). This has led that can and that cannot support growth (for a few examples, 3990 Appl Microbiol Biotechnol (2019) 103:3979–4002

Fig. 3 Schematic distribution of the known pathways for aromatic substituted aromatic compounds down to the different catabolic nodes catabolism currently indexed in the eLignin database. Please note that from where ring fission occurs (here called fission pathways). The three this representation should be seen as a hypothetical map of the existing routes that funnel compounds derived from the primary monolignols (S, possibilities within aromatic catabolism, and not as a map of a H, G) are indicated in dotted boxes: the sinapyl (S), p-coumaryl (H), and Bsuperbug.^ Funneling pathways refer to routes that reduce larger/more coniferyl (G) branches see Bache and Pfennig 1981; Defnoun et al. 2000;Harwood unit; G), and p-coumaryl alcohol (p-hydroxyphenyl unit; H) and Gibson 1988; Song 2009) and thereby present a valuable (Vanholme et al. 2010). The ratio of units in the polymer hint to which funneling pathways can and cannot be expected differs depending on the lignin source, with softwood in the organism. At the moment, the indexing in eLignin has consisting of mainly G units with a small fraction of H units, been focused on the substrates that can be used, but a logical hardwood having a combination of almost exclusively S and next step for the database development is to also include sub- G, and monocots all three (Gellerstedt and Henriksson 2008; strates that an organism cannot use. Gosselink et al. 2010). Recent reports have also shown that a caffeyl alcohol homopolymer (caffeyl unit; C) can be found in Prediction of funneling pathway distributions seed coats of, e.g., vanilla orchard and some cacti species (Barsberg et al. 2018;Chenetal.2012a). Consequently, the Lignin consists of three primary building blocks known as composition of aromatics in the depolymerized lignin will monolignols that plants produce from the amino acid phenyl- differ greatly between different lignocellulose feedstocks. alanine: sinapyl alcohol (called syringyl, or S, unit when in- Following the S, G, and H types, three main funneling corporated in the lignin polymer), coniferyl alcohol (guaiacyl pathways for monoaromatic catabolism have been defined, Appl Microbiol Biotechnol (2019) 103:3979–4002 3991

a 4-hydroxybenzoic acid -70 vanillic acid - 65 ferulic acid - 48 benzoic acid - 47 catechol - 44 phenol - 43 protocatechuic acid - 43 10 10 12 11 70 vanillin - 42 14 13 14 Kraft lignin - 35 15 15 65 resorcinol - 24 15 p-coumaric acid - 23 15 alkali lignin - 20 15 48 hydroquinone - 19 16 guaiacol - 19 16 syringic acid - 18 17 cinnamic acid - 18 47 benzaldehyde - 18 18 3-hydroxybenzoic acid - 17 18 caffeic acid - 16 anisoin - 16 18 44 dehydropolymerisate (DHP) - 15 19 biphenyl - 15 phenylacetic acid - 15 19 43 20 corn stover lignin - 15 phenylacetic acid - 15 23 43 salicylic acid - 14 24 35 42 benzylvanillin -14 gallic acid -13 Klason lignin - 12 veratryl alcohol - 11 gentisic acid - 10 p-cresol - 10

b Proteobacteria Actinobacteria Firmicutes Bacteroidetes Ascomycota Basidiomycota Euryarchaeota 35 33

25 25 22

20 18

15 12 12 11 Number of Number of strains 10 9 7 7 6 5 3 3 3 2 1 1 0 000 0 Natural lignins Technical lignins Di- and oligomers Fig. 4 a Substrates that can be utilized by > 10 organisms listed in the species that can degrade natural and technical lignins, and di- and oligo- database; the numbers represent the number of strains in the database that meric aromatic compounds, sorted by phylum. To distinguish the bacteria utilize each compound. Total number of substrates that satisfied the > 10 from the representatives of the other two kingdoms, the fungal phyla are cutoff—32; total number of substrates in dataset—141. b Number of presented with stripes and the only archaeal phylum is in solid black

based on which of the main lignin units (or derivatives there- branch (no methoxy groups) (see Fig. 3). Within eLignin, of) they catabolize: the sinapyl branch (two methoxy groups), these branches were further divided into one or more sequen- coniferyl branch (one methoxy group), and the p-coumaryl tial pathways in order to better specify which reactions a 3992 Appl Microbiol Biotechnol (2019) 103:3979–4002 species have been characterized with, i.e., a bacteria with a in the dataset (Fig. 5). Another observation is that metabolites of vanillin degradation pathway will not necessarily have the the resorcinol branch (Fig. 3)seemtobedegradedbyfungitoa pathway for ferulic acid, although these pathways are sequen- larger extent than the other branches according to the current tial in the coniferyl branch. Microbial aromatic catabolism is data (Fig. 5). Resorcinols are part of the phenolics in plants and also not limited to the S, G, and H funneling branches, mean- soil humic acids (Burges et al. 1964;Klugeetal.1990) and do ing that there is a need for naming of other routes as well, not seem to be derived from lignin per se, which would put this including aromatics that are derived from other origins than compound within niche subgroup 2. lignins (e.g., other plant matter). Some examples include the caffeic acid, benzoyl, resorcinol, and cresol pathways (Fig. 3). Predicting organisms that can catabolize a given Funneling pathways for di- and oligomeric aromatics, the depolymerization mix study of which has started emerging in certain species (Bugg et al. 2011b;Kamimuraetal.2017), is another example of Many lignin valorization studies apply chemical depolymeri- essential catabolic routes. zation since microbial enzymatic breakdown of lignin is a In a lot of bibliome studies, the substrate specificity of a very slow process taking many weeks (Fackler et al. 2006; species is presented without going into the intracellular con- Hedges et al. 1988; Liers et al. 2011). Therefore, from an version mechanisms nor reporting evidence of a specific applied point-of-view, it would be of interest to run the pre- funneling pathway. Therefore, in order to be able to use the diction model Bbackwards^ in order to identify which organ- eLignin dataset to look at pathway diversity, we developed a ism(s) would be likely to grow on the mixture of aromatic prediction algorithm to infer funneling branches from reported monomers resulting from chemical depolymerization. The substrates from the literature. This is possible since many of outcome of the depolymerization is highly dependent on pro- the funneling branches are linear, e.g., ferulic acid is degraded cess conditions and lignin source (Sun et al. 2018), and via vanillin, and any species that have been reported to grow predicting the monomeric yield is beyond the scope of this on these compounds and their intermediates can then be the- review. However, the distribution of H, G, and S units in a oretically inferred to have the coniferyl branch (Fig. 3). given lignin might be indicative of the possible monomeric Cinnamic acid is reported to be catabolized by 18 organisms composition in the depolymerisate. Using this assumption, (Fig. 4a), but due to the alternate metabolic routes for its deg- depolymerized softwood lignin would need microbes with radation—e.g., via benzoic acid, 3-phenylpropionic acid, or funneling pathways for coniferyl- (G) and p-coumaric (H)- styrene (Chamkha et al. 2001; Defnoun et al. 2000;Monisha derived monomers. Spruce lignosulfonate has for instance et al. 2018; Mäkelä et al. 2015)—it was omitted from the been reported to yield vanillin, guaiacol, acetovanillone, and prediction model. Also, according to current knowledge, an- vanillic acid (Pérez and Tuck 2018). Some examples of organ- aerobic aromatic catabolism frequently (but not exclusively) isms that can catabolize both vanillic acid and guaiacol in- relies on pathways that converge on benzoyl-CoA, that is clude Amycolatopsis sp. ATCC 39116 (Pometto III et al. further subjected to ATP-dependent hydrolysis to open the 1981), Comamonas sp. B-9 (Chen et al. 2012c), and aromatic ring (Durante-Rodríguez et al. 2018; Fuchs et al. Rhodotorula rubra IFO 889 (Huang et al. 1993). Hardwood 2011); but since the exact mechanisms are largely unknown depolymerisates would require species that can handle mono- for the species in the dataset, all anaerobic microbes have been mers derived from S and G units, and therefore, organisms put in an Banaerobic branch (es)^ cluster (Fig. 5). with the syringyl (S) and coniferyl (G) branches would be The result of the theoretical prediction is presented in Fig. 5. needed, such as Sphingobium sp. SYK-6 (Katayama et al. The main conclusion is that, of the three main funneling 1988), Acetobacterium woodii NZva16 (Bache and Pfennig branches (S, G, H), the coniferyl (G) and p-coumaric (H) 1981), or Rhizobium sp. YS-1r (Jackson et al. 2017). Species branches seem by far to be the most abundant in niche 2. This that seem able to degrade compounds from all the S, G, and H might be correlated to the number of methoxy groups (none in branches, which would be representative of grass lignins, the H unit, one in the G unit, two in the S unit; Fig. 3), as ring would include Oceanimonas doudoroffii JCM21046T fission usually seems to occur after the methoxy groups have (Numata and Morisaki 2015)andExophiala jeanselmei CBS been demethylated to hydroxyl groups (Gupta et al. 1986; 658.76 (Middelhoven 1993). Please note that these predic- Nishikawa et al. 1998;Sampaio1999). As the demethylation tions do not take culture and process conditions into account, often requires a cofactor such as tetrahydrofolic acid (Masai meaning that some of these species might be better suited for et al. 2004) and NADH and FAD (Mallinson et al. 2018), the process applications than others. degradation of methylated aromatics may be limited by the rate of cofactor recycling. Furthermore, it is noteworthy that there is Transport proteins no caffeic acid degrading Actinobacteria yet in the eLignin database, despite the fact that they are the prokaryotic phylum Although the chemical structure of many aromatic com- that is commonly the second most abundant for most branches pounds allow them to passively diffuse through the lipid Appl Microbiol Biotechnol (2019) 103:3979–4002 3993

100

90 Euryarchaeota

80 Basidiomycota 70 Ascomycota 60 Acidobacteria 50 Spirochaetes 40 Bacteroidetes

Number of Number of strains 30 Firmicutes 20 Actinobacteria Proteobacteria 10 0

Fig. 5 Distribution of putative funneling pathway branches in the eLignin distinguish the bacteria from the representatives of the other two king- bibliome, inferred from reported substrates, sorted by phylum. Because of doms, the fungal phyla are presented with stripes and the only archaeal the overall linear nature of the aerobic funneling pathways (Fig. 3), it is phylum is in solid black. A detailed outcome of the prediction for each possible to use the substrates reported in the literature for a given organ- species with links to the different references is found online at www. ism and correlate that to a funneling pathway branch (i.e., a collection of elignindatabase.com under each organism entry page. Please note that funneling pathways). The small group of species that has been reported to the results are theoretical and it is up to everyone to assess the degrade aromatics anaerobically has all been clustered in the anaerobic probability of these inferences, e.g., by reading the primary references branch in order not to generate false positives in the other branches. To for each organism bilayers of biological membranes (Engelke et al. 1996), many by active transporters and not by diffusion in many species. microorganisms have dedicated transport channels or proteins This may be explained by the fact that these compounds are for aromatic compounds—reviewed, e.g., by Parales and by commonly protonated at neutral pH and—due to the hydro- Kamimura and their colleagues (Kamimura et al. 2017; phobic charge—can partition into the membrane and damage Parales and Ditty 2017; Parales et al. 2008). In fact, transporter the structure (Kamimura et al. 2017; Parales and Ditty 2017). genes are commonly found within the catabolic operons for Gram-negative bacteria with reported aromatic transporters aromatic acids (Parales et al. 2008) which could suggest that include Acinetobacter baylyi ADP1 (Collier et al. 1997; the natural diffusion rate of certain aromatics is too limited for D’Argenio et al. 1999), Bradyrhizobium japonicum growth on aromatics as a sole carbon source. Transporters are USDA110 (Michalska et al. 2012), Klebsiella pneumoniae of interest for metabolic engineering purposes, as a part of M5a1 (Xu et al. 2012), Pseudomonas putida KT2440 uptake optimization and/or expansion of the substrate range (Nishikawa et al. 2008) and PRS2000 (Nichols and of a given strain. As more and more of the metabolic pathways Harwood 1997), Rhodopseudomonas palustris CGA009 for aromatic degradation are now elucidated, there seems to be (Giuliani et al. 2011; Michalska et al. 2012), Sinorhizobium an emerging effort within the fundamental molecular biology meliloti 1024 (Michalska et al. 2012), and Sphingobium sp. studies on lignin degradation to look into transport proteins. SYK-6 (Mori et al. 2018). Gram-positives, on the other hand, We have begun indexing transport proteins as part of the or- only have a single cell membrane in their envelope: the cyto- ganism pages in eLignin, and we anticipate that this section plasmic membrane (Parales and Ditty 2017). There seem to be will grow as this field expands. less studies on Gram-positive than Gram-negative species Current knowledge on bacterial aromatic transporters with regard to aromatic transport. Some examples include mostly focuses on Gram-negative bacteria which have a cell Corynebacterium glutamicum ATCC 13032 (Chaudhry et al. envelope with two lipid bilayers separated by a periplasmic 2007;Xuetal.2006), Lactobacillus plantarum WCFS1 space: the outer and the inner membrane (Nikaido 2003). (Reverón et al. 2017), and Rhodococcus jostii RHA1 (Otani Some Gram-negatives have been reported to have substrate- et al. 2014). It is also worthwhile to note that in addition to the specific diffusion channels for aromatic compounds on the mechanisms for transport of aromatics into the cell, many outer membrane (Hearn et al. 2008; Nikaido 2003). Inner species also have efflux pumps in order to cope with the often membrane transport of aromatic acids seems to be achieved cytotoxic properties of aromatic compounds (Parales and 3994 Appl Microbiol Biotechnol (2019) 103:3979–4002

Ditty 2017), or as a means to excrete detoxified compounds. and thus become an operational tool for studies on the micro- Ravi and colleagues have for instance described a biological aspect of lignin degradation, catabolism, and Pseudomonas isolate that excreted vanillyl alcohol during valorization. growth on vanillin as a tolerance mechanism to handle excess vanillin that was not catabolized to vanillic acid fast enough, Acknowledgements The authors would like to thank Javier García- but the mechanism by which vanillyl alcohol was transported Hidalgo for his contributions to the initial data mining performed before the construction of the database. out of the cell has not been elucidated yet (Ravi et al. 2018). Availability of data and materials The database is available online at www.elignindatabase.com, with no restrictions for academic or non- Conclusions and outlook academic use. The eLignin Database: Copyright 2016–-2019 Daniel Brink, Applied Microbiology, Department of Chemistry, Lund University, Sweden. We welcome contributions to the database; instruc- The interest for lignin as an underexploited carbon source has tions are available at the homepage. All contributions will undergo man- markedly increased during the last two decades, as evidenced ual curation. by the exponential increase in published papers on lignin val- ’ orization (Abejón et al. 2018). In this minireview, we used our Authors contributions DB designed the study, designed and pro- grammed the database and web interface, performed the data mining, recently created resource, the eLignin database, to analyze the wrote the manuscript, and curated the database content. KR assisted in diversity of the lignin microbial niche, which we have defined the data mining and curation. GL and MGG conceived the study and as all microbes that can either degrade lignin or lignin-derived revised the manuscript. All authors read and approved the final aromatic compounds. It should, however, be kept in mind that manuscript. the data in eLignin encompasses the diversity in the bibliome, Funding This work was financed by the Swedish Foundation for meaning that it reflects what people have reported in the liter- Strategic Research through the grant contract RBP14-0052. ature. The papers that are indexed in the database concern microbial isolates, i.e., species that were cultivable. It is, there- Compliance with ethical standards fore, inevitable that this approach does not represent the overall diversity of the lignin microbial niche, as there are many Competing interests The authors declare that they have no competing species within the niche community that cannot be detected interests. and sustained with the common isolation methodologies. Open Access This article is distributed under the terms of the Creative Although the aim of this minireview is to show the diversity Commons Attribution 4.0 International License (http:// of the niche, it also reveals the diversity and fashions within creativecommons.org/licenses/by/4.0/), which permits unrestricted use, the scientific community, which may or may not correlate with distribution, and reproduction in any medium, provided you give appro- the biological diversity. We can also conclude that the litera- priate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. ture is enriched with physiological characterization, i.e., aromatic substrate specificities of different organisms are rather well known. The molecular biology of specific metabolic References routes is, in contrast, less well elucidated, which will be an important next step both for the fundamental understanding of Abdelaziz OY,Brink DP, Prothmann J, Ravi K, Sun M, García-Hidalgo J, the biology and for the many projects that apply microbes in a Sandahl M, Hulteberg CP, Turner C, Lidén G, Gorwa-Grauslund value chain for lignin valorization. The prediction algorithm MF (2016) Biological valorization of low molecular weight lignin. Biotechnol Adv 34(8):1318–1346 for aromatic pathways presented in this review can hopefully Abejón R, Pérez-Acebo H, Clavijo L (2018) Alternatives for chemical generate new hypotheses on the molecular biology of the and biochemical lignin valorization: hot topics from a bibliometric niche and pave the way for future studies. analysis of the research published during the 2000–2016 period. The microbiological aspects of lignin and aromatics degra- Processes 6(8):98 Acevedo F, Pizzul L, Castillo MD, Cuevas R, Diez MC (2011) dation have a long history with a vast bibliome, and the need Degradation of polycyclic aromatic hydrocarbons by the Chilean for resources such as the eLignin database will continue to white-rot fungus Anthracophyllum discolor.JHazardMater grow as the field expands. In the future, we expect to further 185(1):212–219. https://doi.org/10.1016/j.jhazmat.2010.09.020 implement in eLignin a number of discussed features includ- Acland A, Agarwala R, Barrett T, Beck J, Benson DA, Bollin C, Bolton E, Bryant SH, Canese K, Church DM (2014) Database resources of ing improved prediction algorithms, lignolytic communities, the National Center for Biotechnology Information. Nucleic Acids and substrates that cannot be converted by a given organism. Res 42(Database issue):D7 Economically feasible lignin valorization will require ad- Alexieva Z, Yemendzhiev H, Zlateva P (2010) Cresols utilization by vanced metabolic engineering and thorough knowledge on Trametes versicolor and substrate interactions in the mixture with – microbial physiology. In that context, the objective of phenol. Biodegradation 21(4):625 635 Antai SP, Crawford DL (1981) Degradation of softwood, hardwood, and eLignin is not only to generate new overviews of the field grass lignocelluloses by two Streptomyces strains. Appl Environ but also to fuel new research ideas and engineering strategies Microbiol 42(2):378–380 Appl Microbiol Biotechnol (2019) 103:3979–4002 3995

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